Dynamic changes in primate endometrial leukocyte populations: Differential distribution of macrophages and natural killer cells at the rhesus monkey implantation site and in early pregnancy

Placenta

Volumn 25, Issue 4, 2004, Pages 297-307

  Slukvin, I I ^a,b   Breburda, E E ^a   Golos, T G ^a,c  

^a UNIVERSITY OF WISCONSIN   (United States)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CD3 ANTIGEN; CD56 ANTIGEN; CD68 ANTIGEN;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL AGGREGATION; CELL COUNT; CELL FUNCTION; CELL POPULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOTROPHOBLAST; DECIDUA; ENDOMETRIUM; FEMALE; FIRST TRIMESTER PREGNANCY; IMMUNOHISTOCHEMISTRY; LEUKOCYTE; MACROPHAGE; MENSTRUAL CYCLE; NATURAL KILLER CELL; NIDATION; NONHUMAN; PLACENTA DEVELOPMENT; PRIMATE; PRIORITY JOURNAL; RHESUS MONKEY; T LYMPHOCYTE; TROPHOBLAST;

EID: 1942487682     PISSN: 01434004     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.placenta.2003.08.019     Document Type: Article

References (68)

1. Bulmer JN, Longfellow M, Ritson A. Leukocytes and resident blood cells in endometrium. Ann N Y Acad Sci 1991;622:57-68.
2. Hunt JS. Immunologically relevant cells in the uterus. Biol Reprod 1994; 50:461-6.
3. Whitelaw PF, Croy BA. Granulated lymphocytes of pregnancy. Placenta 1996;17:533-43.
4. Ito K, Karasawa M, Kawano T, Akasaka T, Koseki H, Akutsu Y et al. Involvement of decidual Valpha14 NKT cells in abortion. Proc Natl Acad Sci U S A 2000;97:740-4.
5. Hunt JS, Petroff MG, Burnett TG. Uterine leukocytes: key players in pregnancy. Semin Cell Dev Biol 2000;11:127-37.
6. Bulmer JN, Morrison L, Smith JC. Expression of class II MHC gene products by macrophages in human uteroplacental tissue. J Immunol 1988;63:707-14.
7. Tachi C, Tachi S, Knyszynski A, Lindner HR. Possible involvement of macrophages in embryo-maternal relationships during ovum implantation in the rat. J Exp Zool 1981;217:81-92.
8. Pollard JW, Hunt JS, Wiktor-Jedrzejczak W, Stanley ER. A pregnancy defect in the osteopetrotic (op/op) mouse demonstrates the requirement for CSF-1 in female fertility. Dev Biol 1991;148:273-83.
9. King BF, Blankenship TN. Development and organization of primate trophoblast cells. In: Soares MJ, Handwerger S, Talamantes F, editors. Trophoblast cells. New York: Springer-Verlag; 1993, p. 13-30.
10. Enders AC, Blankenship TN, Fazleabas AT, Jones CJP. Structure of anchoring villi and the trophoblastic shell in the human, baboon and macaque placenta. Placenta 2001;22:284-303.
11. Slukvin II, Watkins DI, Golos TG. Phenotypic and functional characterization of rhesus monkey decidual lymphocytes: rhesus decidual large granular lymphocytes express CD56 and have cytolytic activity. J Reprod Immunol 2001;50:57-79.
12. Enders AC, King BF. Early stages of trophoblastic invasion of the maternal vascular system during implantation in the macaque and baboon. Am J Anat 1991;192:329-46.
13. Golos TG, Handrow RR, Durning M, Fisher JM, Rilling JK. Regulation of chorionic gonadotropin-alpha and chorionic somatomammotropin messenger ribonucleic acid expression by 8-bromo-adenosine 3′, 5′-monophosphate and dexamethasone in cultured rhesus monkey syncytiotrophoblasts. Endocrinology 1992; 131:89-100.
14. Slukvin II, Boyson JE, Watkins DI, Golos TG. The rhesus monkey analog of HLA-G is expressed primarily in villous syncytiotrophoblasts. Biol Reprod 1998;58:728-38.
15. Kelly PM, Bliss E, Morton JA, Burns J, McGee JO. Monoclonal antibody EBM/11: high cellular specificity for human macrophages. J Clin Pathol 1988;41:510-5.
16. Ringler DJ, Walsh DG, MacKey JJ, Hunt RD, King NW. Immunophenotypic characterization of mononuclear phagocytes and dendritic cells in lymphoid organs of the rhesus monkey. Clin Immunol Immunopathol 1988;49:349-64.
17. Bulmer JN. Human endometrial lymphocytes in normal pregnancy and pregnancy loss. Ann N Y Acad Sci 1994;734:185-92.
18. Zimmer MI, Larregina AT, Castillo CM, Capuano S III, Falo Jr LD, Murphey-Corb M et al. Disrupted homeostasis of Langerhans cells and interdigitating dendritic cells in monkeys with AIDS. Blood 2002; 99:2859-68.
19. Nooij FJ, Jonker M, Balner H. Differentiation antigens on rhesus monkey lymphocytes. II. Characterization of RhT3, a CD3-like antigen on T cells. Eur J Immuno 1986;16:981-4.
20. Blankenship TN, Enders AC. Trophoblast cell-mediated modifications to uterine spiral arteries during early gestation in the macaque. Acta Anat 1997;158:227-36.
21. Slukvin II, Lunn DP, Watkins DI, Golos TG. Placental expression of the non-classical MHC Class I molecule Mamu-AG at implantation in the rhesus monkey. Proc Natl Acad Sci U S A 2000;97:9104-9.
22. Zhou LJ, Schwarting R, Smith HM, Tedder TF. A novel cell-surface molecule expressed by human interdigitating reticulum cells, Langerhans cells, and activated lympocytes is a new member of the Ig superfamily. J Immunol 1992;149:735-42.
23. Zhou LJ, Tedder TF. Human blood dendritic cells selectively express CD83, a member of the immunoglobulin superfamily. J Immunol 1995; 154:3821-35.
24. Kammerer U, Schoppet M, McLellan AD, Kapp M, Huppertz HI, Kampgen E et al. Human decidua contains potent immunostimulatory CD83(+). Am J Pathol 2000;157:159-69.
25. Dougherty GJ, Selvendran Y, Murdoch S, Palmer DG, Hogg N. The human mononuclear phagocyte high-affinity Fc receptor, FcRI, defined by a monoclonal antibody, 10.1. Eur J Immunol 1987;17:1453-9.
26. Brans YW, Kuehl TJ. Non-human primates in perinatal research. New York: John Wiley & Sons, Inc, 1988 472 pp.
27. Loke YW, King A. Human implantation. Cell biology and imunology. Cambridge: Cambridge University Press, 1995.
28. Bulmer JN, Johnson PM. Macrophage populations in the human placenta and amniochorion. Clin Exp Immunol 1984;57:393-403.
29. Redline RW, Lu CY. Localization of fetal major histocompatibility complex antigens and maternal leukocytes in routine placenta. Implications for maternal-fetal immunological relationship. Lab Invest 1989;61:27-36.
30. Chen HL, Yang YP, Hu XL, Yelavarthi KK, Fishback JL, Hunt JS. Tumor necrosis factor alpha mRNA and protein are present in human placental and uterine cells at early and late stages of gestation. Am J Pathol 1991;139:327-35.
31. Todt JC, Yang Y, Lei J, Lauria MR, Sorokin Y, Cotton DB et al. Effects of tumor necrosis factor-alpha on human trophoblast cell adhesion and motility. Am J Reprod Immunol 1996;36:65-71.
32. Defilippi P, Silengo L, Tarone G. Alpha 6 beta 1 integrin (laminin receptor) is down-regulated by tumor necrosis factor alpha and interleukin-1 beta in human endothelial cells. J Biol Chem 1992; 267:18303-7.
33. Schneider P, Tschopp J. Apoptosis induced by death receptors. Pharmaceutica Acta Helvetiae 2000;74:281-6.
34. Yui J, Hemmings D, Garcia-Lloret M, Guilbert LJ. Expression of the human p55 and p75 tumor necrosis factor receptors in primary villous trophoblasts and their role in cytotoxic signal transduction. Biol Reprod 1996;55:400-9.
35. Chen HL, Yelavarthi KK, Hunt JS. Identification of transforming growth factor-beta 1 mRNA in virgin and pregnant rat uteri by in situ hybridization. J Reprod Immunol 1993;25:221-33.
36. Rizzino A. Transforming growth factor-beta: multiple effects on cell differentiation and extracellular matrices. Dev Biol 1988;130:411-22.
37. Irving JA, Lala PK. Functional role of cell surface integrins on human trophoblast cell migration: regulation by TGF-beta, IGF-II, and IGFBP-1. Exp Cell Res 1995;217:419-27.
38. Colonna M, Samaridis J, Cella M, Angman L, Allen RL, Ocallaghan CA et al. Human myelomonocytic cells express an inhibitory receptor for classical and nonclassical MHC class I molecules. J Immunol 1998; 160:3096-100.
39. Navarro F, Llano M, Bellon T, Colonna M, Geraghty DE, Lopez-Botet M. The ILT2(LIR1) and CD94/NKG2A NK cell receptors respectively recognize HLA-G1 and HLA-E molecules co-expressed on target cells. Eur J Immunol 1999;29:277-83.
40. Petroff MG, Sedlmayr P, Azzola D, Hunt JS. Decidual macrophages are potentially susceptible to inhibition by class Ia and class Ib HLA molecules. J Reprod Immunol 2002;56:3-17.
41. Fanger NA, Cosman D, Peterson L, Braddy SC, Maliszewski CR, Borges L. The MHC class I binding proteins LIR-1 and LIR-2 inhibit Fc receptor-mediated signaling in monocytes. Eur J Immunol 1998; 28:3423-34.
42. Hara N, Fujii T, Yamashita T, Kozuma S, Okai T, Taketani Y. Altered expression of human leukocyte antigen G (HLA-G) on extravillous trophoblast in preeclampsia - immunohistological demonstration with anti-HLA-G specific antibody 87G and anti-cytokeratin antibody CAM5.2. Am J Reprod Immunol 1996;34:349-58.
43. Goldman-Wohl DS, Ariel I, Greenfield C, Hochner-Celnikier D, Cross J, Fisher S et al. Lack of human leukocyte antigen-G expression in extravillous trophoblasts is associated with pre-eclampsia. Mol Hum Reprod 2000;6:88-95.
44. Reister F, Frank HG, Hey IV, Kosanke G, Huppertz B, Schroder W et al. The distribution of macrophages in spiral arteries of the placental bed in pre-eclampsia differs from that in healthy patients. Placenta 1999; 20:229-33.
45. Drake PM, Gunn MD, Charo IF, Tsou CL, Zhou Y, Huang L et al. Human placental cytotrophoblasts attract monocytes and CD56 (bright) natural killer cells via the actions of monocyte inflammatory protein 1alpha. J Exp Med 2001;193:1199-212.
46. Boyson JE, Iwanaga KK, Golos TG, Watkins DI. Identification of a novel MHC class I gene, Mamu-AG in the placenta of primate with an inactivated G locus. J Immunol 1997;159:3311-21.
47. Slukvin II, Watkins DI, Golos TG. Tissue distribution of the mRNA for a rhesus major histocompatibility class Ib molecule, Mamu-AG. Tissue Antigens 1999;53:282-91.
48. Soilleux EJ, Morris LS, Lee B, Pohlmann S, Trowsdale J, Doms RW et al. Placental expression of DC-SIGN may mediate intrauterine vertical transmission of HIV. J Pathol 2001;195:586-92.
49. Soilleux EJ, Morris LS, Leslie G, Chehimi J, Luo Q, Levroney E et al. Constitutive and induced expression of DC-SIGN on dendritic cell and macrophage subpopulations in situ and in vitro. J Leukoc Biol 2002; 71:445-57.
50. Kammerer U, Eggert AO, Kapp M, McLellan AD, Geijtenbeek TBH, Dietl J et al. Unique appearance of proliferating antigen-presenting cells expressing DC-SIGN (CD209) in the decidua of early human pregnancy. Am J Pathol 2003;162:887-96.
51. Geijtenbeek TBH, Kwon DS, Torensma R, van Vliet SJ, van Duijnhoven GCF, Middel J et al. DC-SIGN, a dendritic cell-specific HIV-1-binding protein that enhances trans-infection of T cells. Cell 2000;100:587-97.
52. Heikkinen J, Mottonen M, Komi J, Alanen A, Lassila O. Phenotypic characterization of human decidual macrophages. Clin Exp Immunol 2003;131:498-505.
53. Tekelioglu-Uysal M, Edwards RG, Kisnisci HA. Ultrastructural relationships between decidua, trophoblast and lymphocytes at the beginning of human pregnancy. J Reprod Fert 1975;42:431-8.
54. Enders AC. Current topic: structural responses of the primate endometrium to implantation. Placenta 1991;12:309-25.
55. Jones CJP, Aplin JD, Fazleabas AT. Decidual stromal cell-lymphocyte interactions in pregnancy. Placenta 2001;22:380-2.
56. Hunt JS, Orr HT. HLA and maternal-fetal recognition. FASEB J 1992; 6:2344-8.
57. Le Bouteiller P. HLA class I chromosomal region, genes, and products: facts and questions. Crit Rev Immunol 1994;14:89-129.
58. Parham P. Immunology: keeping mother at bay. Curr Biol 1996; 6:638-41.
59. Loke YW, King A. Decidual natural-killer-cell interaction with trophoblast: cytolysis or cytokine production? Biochem Soc Trans 2000; 28:196-8.
60. Guimond MJ, Wang B, Croy BA. Engraftment of bone marrow from severe combined immunodeficient (SCID) mice reverses the reproductive deficits in natural killer cell-deficient tg epsilon 26 mice. J Exp Med 1998; 187:217-23.
61. Ashkar AA, Croy BA. Interferon-gamma contributes to the normalcy of murine pregnancy. Biol Reprod 1999;61:493-502.
62. Hunt JS, Miller L, Vassmer D, Croy BA. Expression of the inducible nitric oxide synthase gene in mouse uterine leukocytes and potential relationships with uterine function during pregnancy. Biol Reprod 1997; 57:827-36.
63. Li XF, Charnock-Jones DS, Zhang E, Hiby S, Malik S, Day K et al. Angiogenic growth factor messenger ribonucleic acids in uterine natural killer cells. J Clin Endocrinol Metab 2001;86:1823-34.
64. + lymphocytes from first trimester human decidua using two-color flow cytometry. Am J Reprod Immunol 1993; 29:5-16.
65. Vassiliadou N, Bulmer JN. Quantitative analysis of T lymphocyte subsets in pregnant and non-pregnant human endometrium. Biol Reprod 1996; 55:1017-22.
66. Vassiliadou N, Bulmer JN. Characterization of tubal and decidual leukocyte populations in ectopic pregnancy - evidence that endometrial granulated lymphocytes are absent from the tubal implantation site. Fertil Steril 1998;69:760-7.
67. Proll J, Bensussan A, Goffin F, Foidart JM, Berrebi A, Le Bouteiller P. Tubal versus uterine placentation: similar HLA-G expressing extravillous cytotrophoblast invasion but different maternal leukocyte recruitment. Tissue Antigens 2000;56:479-91.
68. Stock RJ. Histopathologic changes in tubal pregnancy. J Reprod Med 1985;30:923-8.